The abrupt origin and rapid diversification of the flowering plants during the Cretaceous has long been considered an “abominable mystery.” While the cause of their high diversity has been attributed largely to coevolution with pollinators and herbivores, their ability to outcompete the previously dominant ferns and gymnosperms has been the subject of many hypotheses. Common among these is that the angiosperms alone developed leaves with smaller, more numerous stomata and more highly branching venation networks that enable higher rates of transpiration, photosynthesis, and growth. Yet, how angiosperms pack their leaves with smaller, more abundant stomata and more veins is unknown but linked—we show—to simple biophysical constraints on cell size. Only angiosperm lineages underwent rapid genome downsizing during the early Cretaceous period, which facilitated the reductions in cell size necessary to pack more veins and stomata into their leaves, effectively bringing actual primary productivity closer to its maximum potential. Thus, the angiosperms' heightened competitive abilities are due in no small part to genome downsizing.

Author summary

The angiosperms, commonly referred to as the flowering plants, are the dominant plants in most terrestrial ecosystems, but how they came to be so successful is considered one of the most profound mysteries in evolutionary biology. Prevailing hypotheses have suggested that the angiosperms rose to dominance through an increase in their maximum potential photosynthesis and whole-plant carbon gain, allowing them to outcompete the ferns and gymnosperms that had previously dominated terrestrial ecosystems. Using a combination of anatomy, cytology, and modelling of liquid water transport and CO2 exchange between leaves and the atmosphere, we now provide strong evidence that the success and rapid spread of flowering plants around the world was the result of genome downsizing. Smaller genomes permit the construction of smaller cells that allow for greater CO2 uptake and photosynthetic carbon gain. Genome downsizing occurred only among the angiosperms, and we propose that it was a necessary prerequisite for rapid growth rates among land plants.